JXB Advance Access originally published online on July 29, 2009
Journal of Experimental Botany 2009 60(13):3909-3922; doi:10.1093/jxb/erp226
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© 2009 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
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RESEARCH PAPER |
Developmental changes and organelle biogenesis in the reproductive organs of thermogenic skunk cabbage (Symplocarpus renifolius)
1Cryobiofrontier Research Center, Iwate University, Morioka 020-8550, Japan
2RIKEN Plant Science Center, Yokohama, Kanagawa 230-0045, Japan
3Graduate School of Life Sciences, Tohoku University, Sendai 980-8577, Japan
4Faculty of Science, Tohoku University, Sendai 980-8578, Japan
5The 21st Century Center of Excellence Program, Iwate University, Morioka 020-8550, Japan
* To whom correspondence should be addressed: E-mail. ykoito{at}iwate-u.ac.jp
Sex-dependent thermogenesis during reproductive organ development in the inflorescence is a characteristic feature of some of the protogynous arum species. One such plant, skunk cabbage (Symplocarpus renifolius), can produce massive heat during the female stage but not during the subsequent male stage in which the stamen completes development, the anthers dehisce, and pollen is released. Unlike other thermogenic species, skunk cabbage belongs to the bisexual flower group. Although recent studies have identified the spadix as the thermogenic organ, it remains unclear how individual tissues or intracellular structures are involved in thermogenesis. In this study, reproductive organ development and organelle biogenesis were examined during the transition from the female to the male stage. During the female stage, the stamens exhibit extensive structural changes including changes in organelle structure and density. They accumulate high levels of mitochondrial proteins, including possible thermogenic factors, alternative oxidase, and uncoupling protein. By contrast, the petals and pistils do not undergo extensive changes during the female stage. However, they contain a larger number of mitochondria than during the male stage in which they develop large cytoplasmic vacuoles. Comparison between female and male spadices suggests that mitochondrial number rather than their level of activity correlates with thermogenesis. Their spadices, even in the male, contain a larger amount of mitochondria that had greater oxygen consumption, compared with non-thermogenic plants. Taken together, our data suggest that the extensive maturation process in stamens produces massive heat through increased metabolic activities. The possible mechanisms by which petal and pistil metabolism may affect thermogenesis are also discussed.
Key words: Alternative oxidase, bisexual flower, mitochondrial density, respiration, stamen, thermogenesis, thermoregulation, ultrastructure, uncoupling protein, vacuole
These authors contributed equally to this work. Received 18 March 2009; Revised 26 May 2009 Accepted 29 June 2009